Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau

• Published in: Proceedings of the National Academy of Sciences - PNAS 2018-02, Vol.115 (8), p.1865-1870
• Main Authors: Zhu, Xiaojia, Guan, Yuyan, Signore, Anthony V., Natarajan, Chandrasekhar, DuBay, Shane G., Cheng, Yalin, Han, Naijian, Song, Gang, Qu, Yanhua, Moriyama, Hideaki, Hoffmann, Federico G., Fago, Angela, Lei, Fumin, Storz, Jay F.
• Format: Article
• Language: English
• Subjects: Acids; Adaptation; Adaptation, Physiological - genetics; Affinity; Altitude; Amino acids; Animal Distribution; Animals; Biochemistry; Biological evolution; Biological Sciences; Birds; Convergence; Divergence; Evolution, Molecular; Hemoglobin; Hemoglobins - genetics; Hemoglobins - physiology; High altitude; Models, Molecular; Molecules; Mutation; Passeriformes - blood; Passeriformes - genetics; Passeriformes - physiology; Protein Conformation; Protein Isoforms; Site-directed mutagenesis; Species; Tibet
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1720487115

When different species experience similar selection pressures, the probability of evolving similar adaptive solutions may be influenced by legacies of evolutionary history, such as lineage-specific changes in genetic background. Here we test for adaptive convergence in hemoglobin (Hb) function among high-altitude passerine birds that are native to the Qinghai-Tibet Plateau, and we examine whether convergent increases in Hb–O₂ affinity have a similar molecular basis in different species. We documented that high-altitude parid and aegithalid species from the Qinghai-Tibet Plateau have evolved derived increases in Hb–O₂ affinity in comparison with their closest lowland relatives in East Asia. However, convergent increases in Hb–O₂ affinity and convergence in underlying functional mechanisms were seldom attributable to the same amino acid substitutions in different species. Using ancestral protein resurrection and site-directed mutagenesis, we experimentally confirmed two cases in which parallel substitutions contributed to convergent increases in Hb–O₂ affinity in codistributed high-altitude species. In one case involving the ground tit (Parus humilis) and gray-crested tit (Lophophanes dichrous), parallel amino acid replacements with affinity-enhancing effects were attributable to nonsynonymous substitutions at a CpG dinucleotide, suggesting a possible role for mutation bias in promoting recurrent changes at the same site. Overall, most altitude-related changes in Hb function were caused by divergent amino acid substitutions, and a select few were caused by parallel substitutions that produced similar phenotypic effects on the divergent genetic backgrounds of different species.